Affiliation

Abstract

Neurons coding for head-direction are crucial for spatial navigation. Here we explored the cellular basis of head-direction coding in the rat dorsal presubiculum (PreS). We found that layer2 is composed of two principal cell populations (calbindin-positive and calbindin-negative neurons) which targeted the contralateral PreS and retrosplenial cortex, respectively. Layer3 pyramidal neurons projected to the medial entorhinal cortex (MEC). By juxtacellularly recording PreS neurons in awake rats during passive-rotation, we found that head-direction responses were preferentially contributed by layer3 pyramidal cells, whose long-range axons branched within layer3 of the MEC. In contrast, layer2 neurons displayed distinct spike-shapes, were not modulated by head-direction but rhythmically-entrained by theta-oscillations. Fast-spiking interneurons showed only weak directionality and theta-rhythmicity, but were significantly modulated by angular velocity. Our data thus indicate that PreS neurons differentially contribute to head-direction coding, and point to a cell-type- and layer-specific routing of directional and non-directional information to downstream cortical targets.

(A) Histogram showing the distribution of HD Indices for all PreS neurons which met the HD criteria (n = 186; see Materials and methods). The median HD index is indicated and shown by the red line. Three recordings from putative FS INs contributed weakly-directional responses (blue; see also Figure 2—figure supplement 1). (B) Polar plots showing firing rate as a function of HD for the neuron with the highest HD index (top) and a representative FS IN (bottom; see also Figure 2—figure supplement 1). For the cell shown on the top panel, all spikes (n = 22) were fired within a narrow HD angle (~10 degrees). HD indices and peak firing rates are indicated. (C) Color-coded distribution of preferred direction for all HD cells (n = 186). Each row represents the firing rate of a single neuron (normalized relative to its peak firing rate; red), ordered by the location of their peak firing rates relative to the rat's HD. (D) Spike-trajectory plot for a HD cell, sequentially recorded during passive rotation (‘head-fixed’, HF) and free-behavior (‘freely-moving’, FM). The circular trajectory of the rat’s head during passive rotation is indicated in black, while the rat’s trajectory during free behavior in gray. Spikes fired during head-fixation and free-behavior are indicated as blue and red dots, respectively. (E) Superimposed spike waveforms (top), polar plots showing firing rate as a function of HD (middle) and linear velocities (bottom) computed from the passive rotation (left) and freely-moving session (right) for the recording shown in (E). Note the stability of the spike-shape and the similar HD tuning between the head-fixed and freely-moving session (the Pearson’s correlation coefficient, p value and peak firing rates are indicated). DOI:http://dx.doi.org/10.7554/eLife.14592.007

(A) Morphological reconstruction of a representative layer 3 pyramidal HD cell (dendrites, red; axon, blue). Scale bar: 100 µm. (B) Angular HD (top) and angular speed (bottom) as a function of time. Spikes (red dots) are indicated. Note the sharp tuning to HD. (C) Polar plots showing firing rate as a function of HD for the neuron in (A). Peak firing rate is indicated. (D) Polar plots showing firing rate as a function of HD computed or the two halves of the recording session for the neuron in (A). The Pearson’s correlation coefficient between the two HD tuning curves and peak firing rates are indicated. (E–H) same as A–D but for another neuron. Scale bar: 100 µm. DOI:http://dx.doi.org/10.7554/eLife.14592.009

Blackstad TW. Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. Journal of Comparative Neurology. 1956;105:417–537. doi: 10.1002/cne.901050305.
-
DOI
-
PubMed